Analysis of biological and biochemical parameters of adult male spiny lobsters Jasus lalandii for identification of possible growth predictors

Highlights

• Size and composition of hepatopancreas are potential predictors of male growth.

• Organ size and lipid content shortly before annual moult are most suited predictors.

• Higher values of these parameters correlate with faster subsequent moult increment.

• More research is required to develop a quantitative predictor for growth prediction.

• This growth prediction can be a novel component for stock assessment.

Abstract

Biological body parameters of adult male West Coast rock lobsters, Jasus lalandii, of commercial size were analysed over two years to determine reserve accumulation during two moult (i.e. growth-) cycles. Two fishing areas were compared that were historically known for fast- and slow growth, respectively. In addition, setagenic development for moult stage determination and the biochemistry of the hepatopancreas were investigated from the fast growth area. This information was intended to confirm previously proposed predictors of annual male moult increment and identify potential new ones. Annual moult increments in these areas were determined from tag-and-recapture studies, including the seasons for which reserve accumulation was analysed. Data from the present study were not robust enough to confirm previously proposed predictors from peak accumulation months (March – May). Data arranged per moult stage were also unsuitable for prediction. Further results analysis, however, identified a subset of data that are potentially more useful: Hepatosomatic index HSI (+ 6 %), lipid content (+ 9 % w_w, + 12 % w_D) and lipid per whole hepatopancreas (+ 24 %) are all significantly higher in July 2011 than in July 2010, the last sampled months before the respective annual moult. These differences correlate with a 26 % (0.7 mm) faster growth during subsequent moult in 2011 than in 2010. Aspects of hepatopancreas lipid metabolism in the months prior to moult have therefore the potential to provide simple and robust predictors of growth in adult male J. lalandii. However, more research is required that also includes the months adjacent to July in more than one area and for a longer period than two years.

Introduction

The West Coast rock lobster (WCRL), Jasus lalandii, is a slow-growing, cold- to temperate water palinurid species from the southern African Atlantic coast. Its fishery is one of the most important in South Africa due to its high value (2016 = R 538 m; ∼$40 m) of which 98 % is exported (Fishing Industry Handbook, 2018). Additionally, the fishery is an important provider of employment for about 4 200 people, most of them along the South African west coast where impoverished communities live (DEFF, 2020). The Branch: Fisheries of the respective national governmental Department (currently Department of Environment, Forestry and Fisheries - DEFF) manages the West Coast rock lobster (WCRL) resource per zone (Fig. 1) by means of Total Allowable Catch (TAC) and, more recently, by additional effort control. Other management measures include a defined fishing season and fishing areas, a minimum legal size and a ban on the retention of berried females (Cockcroft and Payne, 1999). Despite these measures, the resource remains under heavy fishing pressure (including substantial poaching) and is heavily depleted (DEFF, 2020). The current harvestable portion of the resource (males above 75 mm carapace length) is estimated to be only 1.8 % of pristine levels (DEFF, 2020). Accordingly, annual catches have declined from a peak of 18 000 t in the early 1950s to about 1 000 t in 2019 (DEFF, 2020). In addition to fishing pressure, environmental influences have impacted the resource including reduced growth rates (Pollock et al., 1997), low-oxygen events that caused mass stranding of lobsters (Cockcroft, 2001) and an eastward shift in lobster distribution (Cockcroft et al., 2008).

To achieve sustainability and rebuild the stock, an operational management procedure (OMP) was introduced in 1997 (Cockcroft and Payne, 1999). The OMP uses abundance indices (commercial Catch per Unit Effort (CPUE) and a fisheries independent abundance index derived from annual monitoring surveys (FIMS)) and male somatic growth rate to set the TAC prior to the start of the fishing season (DEFF, 2020). While the physiological condition of lobster is taken into account indirectly by the OMP, the ability to predict male somatic growth rate using a reliable physiological index would be a valuable improvement to the TAC setting process. This would be novel not only in South African fisheries but also worldwide where the use of physiological indicators as input data for setting catch levels is scarce.

Such indicators can be organ- or body part indices (in relation to each other or to total weight) and biochemical composition of organs. However, such indices are very species- and life stage-specific. Attempts have been made, for instance, to use the ratios of lipid classes (triglycerides vs. cholesterol) in larval American (clawed) lobsters (Harding and Fraser, 1999), the refractive index of haemolymph and weight to carapace length ratio in juvenile Jasus edwardsii (Oliver and MacDiarmid, 2001). Several parameters have been investigated to predict male moult increment in J. lalandii, such as hepatopancreas- and abdominal muscle size and composition, as well as weight to carapace length ratio (Cockcroft, 1997). Results suggested that aspects of biochemical hepatopancreas composition (moisture, lipids, proteins) are promising candidates.

Mature J. lalandii moult and reproduce once a year (Pollock, 1986). Males moult in late spring to early summer (September-December), well before females in late austral autumn to early winter (April-June) and the mating period in winter (July-August)(Heydorn, 1969a). In males, energy accumulation takes place between the annual moulting events and relies on sufficient prey (Cockcroft, 1997). They use 99 % of energy reserves accumulated during intermoult for growth, in contrast to females which use 5 % (Zoutendyk, 1990). While the maturing ovaries of females become a second center of energy accumulation (Harrison, 1990), large energy reserves in males are stored in the hepatopancreas or midgut gland (Cockcroft, 1997). Due to its large relative size (∼30 % of body weight), though, the storage capacity of the abdominal muscle (“tail”) is also substantial (Smith et al., 2004). However, metabolite concentrations in the latter are seasonally less changeable than in the hepatopancreas (Cockcroft, 1997). Main energy metabolites are lipids and proteins but although proteins were previously regarded as the principle energy source in crustaceans (New, 1976), more recent research revealed that crustaceans differ widely in this regard and that lipids play a major role (Sánchez-Paz et al., 2006). Carbohydrate reserves (in the form of glycogen) play a minor role: they are limited in crustaceans and only power short-term high-intensity anaerobic muscle work, such as tail-flip, after phosphagens are used up (England and Baldwin, 1983). In addition, carbohydrates provide structural chitin building blocks (N-acetylglucosamine) for the formation of the exoskeleton, which are not available for energy production (Charmantier-Daures and Vernet, 2004).

As in other decapods, the hepatopancreas is particularly relevant for many biological processes in palinurids and it is their main organ for lipid digestion and accumulation (Smith et al., 2004; Perera and Simon, 2015; Munian et al., 2020). Its lipid content is therefore high but varies with the moult cycle (Cockcroft, 1997). The lipid deposits in the hepatopancreas serve growth and the formation of the new exoskeleton. Therefore, the peak lipid storage period has a positive correlation to the measured growth increment and was proposed as a potential reliable indicator for growth in males, whereas for proteins, no such relationship was found (Cockcroft, 1997). A reduced level of lipid accumulation during intermoult by the species was shown to lead to low growth rates and even shrinkage (Cockcroft and Goosen, 1995; Cockcroft, 1997). Since reserve accumulation in male WCRL is almost exclusively aimed at providing energy and structural metabolites for moulting, it is helpful to link these processes to distinct stages in the moult cycle. Moult stage was previously determined by the subjective hardness of the exoskeleton and divided into four “hard shell- and soft shell states” (Heydorn, 1969a). This is more practical but less exact than analysis of titres of moulting hormone or setagenic analysis (Marco, 2012). Additional information on these processes in J. lalandii throughout fishing- and moulting seasons would aid understanding of what determines growth increment at the next moult. This is because the current state of knowledge on direct and indirect environmental factors, such as food availability, that impact growth and reproduction of the WCRL is, as described above, suboptimal for predicting population- and resource development and, in turn, sustainable management. In particular, the impact during the reserve accumulation phase is important, because starvation or sub-optimal food supply may impact biological events (moult, spawning) long before they happen.

Historically, growth rates of WCRL of commercial size differ from area to area (Cockcroft and Goosen, 1995). It was found, for example, that there is a substantial difference between two catch areas in close proximity along the Cape Peninsula (about 30 km apart): Olifantsbos and Hout Bay. In Olifantsbos, growth rates have been substantially lower than in Hout Bay since the early 1990s and the two sites were therefore compared previously (Cockcroft, 1997). Such regional growth differences are assumed to be caused by variations in food availability and composition (Newman and Pollock, 1974; Melville-Smith et al., 1995; Chandrapavan et al., 2009, 2010).

The aims of this study were to determine and compare the seasonal variation in the biological cycles (moult and somatic growth rate) and biochemical composition of male lobsters from a high growth (Hout Bay) and low growth (Olifantsbos) area and to determine the potential for the development of a reliable physiological index to predict male somatic growth.